nov., a new Ganodermataceae species from Vietnam: Evidence from morphology and ITS DNA barcodes Xuan Tham Le&Quoc Hung Nguyen Le& Ngoc Duong Pham&Van Hop Duong& Bryn T.. Dentinger&Jean-M
Trang 1ORIGINAL ARTICLE
Tomophagus cattienensis sp nov., a new Ganodermataceae
species from Vietnam: Evidence from morphology
and ITS DNA barcodes
Xuan Tham Le&Quoc Hung Nguyen Le&
Ngoc Duong Pham&Van Hop Duong&
Bryn T M Dentinger&Jean-Marc Moncalvo
Received: 15 April 2011 / Revised: 12 September 2011 / Accepted: 18 September 2011 / Published online: 13 November 2011
# German Mycological Society and Springer 2011
Abstract The polypore genus Tomophagus was created to
segregate one peculiar species, Ganoderma colossum, from
the genus Ganoderma Recent molecular studies have
established the validity of this monotypic genus Here we
report the discovery of a second species of Tomophagus, T
cattienensis sp nov., from Cat Tien National Park in
southern Vietnam, a lowland forest that has been designated
as a Biosphere Reserve by the United Nations Educational, Scientific and Cultural Organization (UNESCO) Recognition
of this new species is based on combined evidence from morphology, cultural characteristics, and ITS rDNA barcodes The discovery of this new species may have implications for the discovery of novel bioactive compounds for pharmaceu-tical use and/or for the pulp industry
Keywords Agaricomycetidae Polyporales Taxonomy Biodiversity
Introduction Ganoderma Karsten and allies (Ganodermataceae Donk, Polyporales, Agaricomycetidae) are a group of polypore fungi of significant economic importance Several species cause severe losses to perennial crops in many tropical countries (Flood et al.2000) and some are of great interest for medicinal and pharmaceutical purposes particularly in eastern Asia (Jong & Birmingham 1992, Lin and Zang
2004) Members of the Ganodermataceae are characterized and easily recognized by the unique presence of double-walled basidiospores The monophyly of the group was confirmed in molecular phylogenetic analyses (Hibbett et
al.1997, Moncalvo et al.2002) However, both generic and specific circumscription within the family has been difficult and controversial (Furtado 1965, Steyaert 1972, 1980, Corner 1983, Zhao 1989, Moncalvo and Ryvarden 1997, Moncalvo 2000)
Murrill (1905a, b) created the genus Tomophagus to segregate G colossum (Fr.) C.F Baker from Ganoderma
Taxonomical novelty: Tomophagus cattienensis Le Xuan Tham & J.
M Moncalvo
X T Le:Q H Nguyen Le
Center for Nuclear Techniques,
Vietnam Atomic Energy Commission,
Ho Chi Minh City, Vietnam
N D Pham
Cat Tien National Park,
Dong Nai Province, Vietnam
V H Duong
Institute for Microorganism and Biotechnology,
National University of Hanoi,
Hanoi, Vietnam
B T M Dentinger ( *):J.-M Moncalvo
Department of Natural History, Royal Ontario Museum, Toronto,
& Department of Ecology and Evolutionary Biology,
University of Toronto,
Toronto, Canada
e-mail: B.Dentinger@kew.org
J.-M Moncalvo
e-mail: jeanmarcm@gmail.com
Present Address:
B T M Dentinger
Jodrell Laboratory, Royal Botanic Gardens,
Kew, Richmond, Surrey TW9 3DS, United Kingdom
DOI 10.1007/s11557-011-0789-3
Trang 2based on its unusually thick and pale context that becomes
soft and light when dry Tomophagus was not accepted by
Furtado (1965), Steyaert (1972, 1980), Corner (1983),
Ryvarden (1991), and many other authors Steyaert (1980)
even suggested that G colossum could be a tropical variant
of the temperate western North American species G
oregonense Murrill that also has a soft and pale context
However, recent molecular phylogenetic studies that used
sequence data from the internal transcribed spacers of the
nuclear ribosomal DNA repeats (ITS rDNA; Moncalvo et al
1995, Moncalvo 2000) and nearly complete mitochondrial
small-subunit ribosomal DNA sequences (Hong and Jung
2004) indicate that G colossum and G oregonense are
distantly related, supporting the recognition of Tomophagus
as a distinct genus
Tomophagus colossus was described by Fries (1851)
from Costa Rica as Polyporus colossus and later transferred
to Ganoderma by Baker (1918) It is a rare species but it
has been reported throughout the tropics, except from East
Africa (Ryvarden and Johansen1980, Ofodile et al.2005)
In Vietnam, T colossus was first recorded by Patouillard
(1897) as G obokense Pat., a species described from
Somalia and later synonymized with G colossum (Furtado
1965, Steyaert 1972, Ryvarden and Johansen 1980,
Ryvarden 2004) This rare species was only recently
rediscovered in Vietnam (Ngo et al.2001)
In this paper we report a second species of Tomophagus
from Cat Tien National Park in southern Vietnam (Cat Tien
is a designated UNESCO Biosphere Reserve; The MAB
Programme 2007) The new species reported here is
distinguished from T colossus on the basis of combined
evidence from morphology, cultural characteristics, and ITS
rDNA barcodes
Materials and methods Organisms studied and morphological examination Four Tomophagus collections were obtained from Vietnam between 2000 and 2008 (Table 1) Macroscopic and anatomical examinations of basidiomata were made as described in Le Xuan Tham (1998) Basidiospore structure was described according to Pegler & Young (1973) and Perreau (1973) Data were compared with the detailed description of the type specimen of T colossus in Steyaert (1972), Ryvarden and Johansen (1980), and Ryvarden (2004) Descriptions of this species in Corner (1983), Gilbertson and Ryvarden (1986), and Wu and Zhang (2003) were also consulted
Cultivation Context tissues from fresh collection of strains CT99, CT119, HCMC10 and ANH s.n were used for isolation in pure culture in a homemade broth of potato-glucose-agar (PGA: Le Xuan Tham et al.1999) Mycelial characteristics were observed on that medium, particularly for the presence/absence of chlamydospores as reported in Peng (1990) In vitro basidioma induction was conducted at room temperature on rubber tree sawdust supplemented with 5% rice bran in 2.5 L plastic bags (Le Xuan Tham et al.1999) DNA analyses
ITS sequences from collections ANH and HCMC10 were produced at the Royal Ontario Museum Sequences from CT99 and CT119 were produced at the DNA sequencing
Table 1 Tomophagus collections used in this study
Species Strain number Origin ITS accession
numbers in the NCBI database
References
Tomophagus colossus CBS 216.36 Philippines; collection C.J Humphrey
no 784; deposited as Ganoderma colossus
by C.J Humphrey, Feb 1936.
Z37071 and Z37091 Moncalvo et al 1995
kk-02 India; ITS sequence obtained from
a BLAST search in Genbank
AJ749970 Sharma et al 2005
ANH s.n (=TRTC 157076) Vietnam; Thua Tien Hue, 2000; NgoAnh s.n JN184395 This work HCMC10 (TRTC 161190) Vietnam; Ho Chi Minh City (Saigon),
District 1, 8 June 2008;
JN184396 This work
Le Xuan Tham & Bryn Dentinger Tomophagus
cattienensis
CT 99 (TRTC 161191) Vietnam; Cat Tien National Park,
6 June 2007;
JN184397 This work P.Ng.Duong & Le Xuan Tham
CT 119 Vietnam; Cat Tien National Park,
2 August 2008;
JN184398 This work P.Ng.Duong & Le Xuan Tham
Trang 3facility of the Institute for Microorganism and Biotechnology,
National Hanoi University A sequence of T colossus CBS
216.36 (Philippines) was retrieved from Moncalvo et al
(1995) A BLAST search in the NCBI database using
TRTC157076 as the query sequence was used to identify
additional sequences from closely related taxa to include in
our dataset Taxa used for DNA analyses are listed in
Table 1, along with their source and GenBank accession
numbers
Sequences were aligned manually and analyzed in
PAUP* (Swofford 2003) using maximum-parsimony and
1,000 nonparametric bootstrap replicates, with 100 heuristic
searches of random addition sequence and TBR
branch-swapping (MP) All gaps in the alignment consisted of
single deletion/insertion and were treated as a "fifth base" in
our analyses Trees were midpoint-rooted
Results and discussion
DNA analyses
BLAST searches returned 99% similarity to Ganoderma sp
kk-02 (AJ749970) from India (Sharma et al 2005), and
<92% similarity to other Ganoderma sequences in the
database Therefore, we only included AJ749970 in our
molecular analyses
After removal of residual SSU and LSU sequences at the
3'-and 5'-end, respectively, ITS sequences were aligned in 558
positions Thirty-five characters were variable, of which 27
were parsimony-informative Maximum-parsimony analysis
returned a single tree of length 35 (CI=1.000, RI=1.000)
Nonparametric bootstrapping strongly supported (100%) the
reciprocal monophyly of T cattienensis sp nov and T
colossus (Fig.1)
Taxonomy
Tomophagus cattienensis Le Xuan Tham & J.M Moncalvo,
spec nov Fig.2
MycoBank no MB 561806
Etymology Named after the locality of the original collections: Cat Tien National Park, Vietnam
Holotype Pham Ngoc Duong & Le Xuan Tham, collection CT99; 6 June 2007; on the trunk of a broad leaf tree, Cat Tien National Park, Dong Nai Province, Vietnam; voucher depos-ited in the mycology herbarium of the Cat Tien National Park; fragments (isotypes) in the Royal Ontario Museum, Toronto, Canada (TRTC 161191), and in the National Museum of Natural Science, Taichung, Taiwan
Distinctus ex Polyporus colossus Fr quo lux lucis rutilus frons superficies, leviter congelo crusta, contextu frons si quando siccus, quod amplus basidiosporae Ordines geno-rum ITS competentes ordinum depositogeno-rum NCBI (GenBank) JN184397
Pileus bulky, thick, flabelliform, dimidiate (~9 cm in diameter and ~8 cm long) with a very short cylindrical stipe, perennial, occurring singly on rotting trunks of hardwood trees Crust red-brown or red-coffeate, laccate at first, but later becoming dull brown by a dusty covering of basidiospores, thin, easily broken when cracking or pressing with fingernails Margin obtuse, rugose, very thick (~3-4 cm), white creamy or pale yellow brown The crust of the stipe is thicker, more laccate, glossy red-brown Context thick ~3.7-7.7 cm, up to
11 cm at the base, homogeneous (without stratifications), soft, light, creamy white becoming pale brown upon drying, somewhat cheesy and powdery, slightly striate above the tubes, composed of dimitic hyphae (generative hyphae hyaline, branched, 2.5-3.5 μm in diameter; skeletal hyphae with thick wall, branched, hyaline, 2–3 μm in diameter) Tube layer thin (0.8-1.4 cm), grey brown to cinnamon brown, unstratified Pores round or angular, small (2-3/mm) with the surface creamy turning pale grey or dark grey when touched Basidiospores typically ganodermoid, honey yellow, 17.5-21.5 x 11.5-14.5 μm, truncate-ovate with a yellow round guttule in the center Basidiospore surface coarse verrucose, pits connected with each other or not completely reticulate (labyrinthine) with thin pillar layer from inner wall Apex (= germpore aperture) hyaline, very thick, concave (truncate) or convex, opposite to the hilum (= the attachment of spore to sterigma) ITS sequence
CBS216.36 Philippines
Kk-02 India Tomophagus
Tomophagus
ANH s.n Vietnam colossus
HCMC10 Vietnam
CT99 Vietnam
100
CT119 Vietnam cattienensis
Fig 1 Phylogenetic tree
result-ing from maximum-parsimony
analyses of Tomophagus ITS
sequences The tree is midpoint
rooted Bootstrap values>70%
are indicated above branches
Trang 4accession number of the type specimen in the NCBI
(GenBank) database: JN184397
Additional specimens examined VIETNAM: Dong Nai
Province, Cat Tien National Park, on the trunk of broad
leaf tree 2 August 2008, Pham Ngoc Duong & Le Xuan
Tham, coll CT119; deposited in the mycology herbarium
of the Cat Tien National Park ITS sequence accession
number in the NCBI (GenBank) database: JN184398
Tomophagus colossus (Fr.) Murrill
The two Vietnamese collections of T colossus examined in
this study (Table1) fully correspond to the morphological
descriptions of the type specimen in Steyaert (1972),
Ryvarden and Johansen (1980), and Ryvarden (2004) In
addition, the collection ANH s.n was described in detail in
Ngo et al (2001) This species is easy to recognize from its thin yellow crust and a pale and chalky context It is rarely found but widespread in the tropics It was reported in the neotropics including Mexico, Florida, and Brazil (Steyaert
1972, Gilbertson and Ryvarden 1986, Gomes-Silva et al
2011), tropical Africa (Steyaert 1972, Ryvarden and Johansen1980), the Arabian Peninsula (Al-Bahry et al
2005), India, Pakistan and Sri Lanka (Steyaert 1972), Malaysia and Indonesia (Corner 1983), and south China and Taiwan (Wu and Zhang 2003) Our ITS analyses also indicate that the strain Ganoderma sp kk-02 reported from India by Sharma et al (2005) corresponds to T colossus Based on the literature cited above, T colossus has a wide host range on woody angiosperms and monocotyledons Wide host range and pantropical distribution of a fungal morphotype is uncommon Future comprehensive studies of this species using mating and molecular data from a broad geographic sampling may reveal the existence of cryptic species within this unique pantropical morphotype Distinction between T cattienensis and T colossus Wild collections of T cattienensis clearly differ morpho-logically from T colossus by having glossy light red-brown basidiomata (rather than yellow), a slightly harder crust, a context that turns pale brown upon drying (instead of remaining creamy white), and slightly larger basidiospores (17.5-21.5 x 11.5-14.5 μm versus 14–20 x 9–14 μm) These characteristics are retained in basidiomata produced
in artificial cultivation (Fig 3) In artificial culture, basidiomata of T cattienensis isolates develop and mature
in 60–75 days, which is 20–25 days longer than for our T colossus strains We also observed difference between the two species in the shape of chlamydospores produced in cultures grown on PGA medium (Fig 3) Tomophagus
Fig 2 Tomophagus cattienensis sp nov.; a wild basidiomata of
collection CT119 (scale bar=10 cm); b wild basidiomata of collection
CT99 (holotype; scale bar=10 cm) - the brown color of the pileus
results from basidiospores deposited on the otherwise reddish crust
(compare with a.) ; c basidiospores of CT99, light microscopy (scale
bar=10 μm); d basidiospores of CT99, hand drawing (scale bar=10
μm); e basidiospores of CT99, SEM (scale bar=10 μm)
Fig 3 Artificial cultivation of Tomophagus cattienensis CT99 (a-c) and
T colossus HCMC10 (d-f); a,d cultures on PGA after 30 days (scale bars=1 cm); b,e chlamydospores formed on PGA (scale bars=10 μm);
f basidiomata produced from sawdust bags (scale bars=5 cm)
Trang 5cattienensis also grows more slowly than T colossus on
PGA medium
Phylogenetic analysis of ITS rDNA barcodes clearly
distinguishes between the two species (Fig.1) MP analyses
yielded a single tree and indicated 100% bootstrap support
for the distinction between T cattienensis and T colossus
Pairwise inter-specific difference was observed in 27–33
nucleotide positions (4.83 - 5.91%), whereas intra-specific
divergence was much lower: the two T cattienensis
collections from Vietnam differ in only six nucleotide
positions (1.08%), and our four Asian samples of T colossus
differ in 1–10 positions (0.18-1.8%) These values for
intra-and inter-specific variation in fungal ITS sequences are in
agreement with the study by Nilsson et al (2008) The
present work therefore confirms the view that ITS can be a
good molecular marker (DNA barcode) for species
identifi-cation in fungi (Seifert2009), although it may not work in all
taxa (Seifert et al.2007, Nilsson et al.2008)
Practical implications of the discovery of T cattienensis
Members of the Ganodermataceae have been shown to be
pharmacologically active and their therapeutic use is being
investigated (Dzubak et al.2006, Liby et al.2007) Recent
studies have reported several new lanostane triterpene
lactones (“colossolactones”) from the cultivated T colossus
strain ANH s.n from Vietnam (Kleinwachter et al.2001, El
Dine et al 2008) Colossactones were also present in a
Nigerian strain of that species (Ofodile et al 2005)
Tomophagus colossus is also known for its excellent
delignification activity (Adaskaveg et al 1990, 1995)
Therefore, the discovery of a novel species of Tomophagus,
T cattienensis, may have implications for the discovery of
novel bioactive compounds for pharmaceutical use and/or
the pulp and biofuel industries
Acknowledgments We thank Dr Ngo Anh (University of Hue,
Vietnam) for providing us with a specimen of T colossus from Thua
Thien Hue Dr Bui Thi Luong (National University of Hanoi) and Ms.
Leena Rivzi (Royal Ontario Museum and University of Toronto)
produced DNA sequence data Mycological research at Cat Tien
National Park was supported by a grant from the Dong Nai Province
Department of Science and Technology to LXT This work was also
supported from the Natural Science and Engineering Research
Council and Genome Canada for funding the Canadian Barcode of
Life Network, and a ROM Fieldwork grant, to JMM.
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